Multi-omic analysis of a hyper-diverse plant metabolic pathway reveals evolutionary routes to biological innovation

Abstract

8The diversity of life on Earth is a result of continual innovations in molecular networks 9 influencing morphology and physiology. Plant specialized metabolism produces hundreds of 10 thousands of compounds, offering striking examples of these innovations. To understand how 11 this novelty is generated, we investigated the evolution of the Solanaceae family-specific, 12 trichome-localized acylsugar biosynthetic pathway using a combination of mass spectrometry, 13 RNA-seq, enzyme assays, RNAi and phylogenetics in non-model species. Our results reveal that 14 hundreds of acylsugars are produced across the Solanaceae family and even within a single plant, 15 revealing this phenotype to be hyper-diverse. The relatively short biosynthetic pathway 16 experienced repeated cycles of innovation over the last 100 million years that include gene 17 duplication and divergence, gene loss, evolution of substrate preference and promiscuity. This 18 study provides mechanistic insights into the emergence of plant chemical novelty, and offers a 19 template for investigating the ~300,000 non-model plant species that remain underexplored. 20 Impact statement 21Integrative analyses of a specialized metabolic pathway across multiple non-model species 22 revealed mechanisms of emergence of chemical novelty in plant metabolism. 23

Advances in Discoveries of Plant Phytochemicals

“…Recently, a series of acylsugar acyltransferases (ASATs) were classified into clade III. The ASATs are produced in type I/IV trichome tip cells and use acetyl or C2-C12 short-chain acyl groups to produce O-acylsugars (Schilmiller et al, 2012;Moghe et al, 2017). In theory, ASATs can produce various compounds, but the ultimate distribution of acylsugars within a species depends on the preferences of ASATs for substrates, which effectively narrows the Maximum-likelihood phylogenetic tree of plant acyltransferases.…”

MetPlast: an R package to evaluate Metabolic Plasticity using Information Theory statistical framework

“…This characteristic does not only apply at the organismal level. In fact, metabolic plasticity might also play a major role in evolutionary processes such as species adaptation, and domestication (Moghe et al, 2017).…”